Histone H1 affects gene imprinting and DNA methylation in Arabidopsis

Rea, Matthew; Zheng, Weihui; Chen, Ming; Braud, Christopher; Bhangu, Drutdaman; Rognan, Tara N.; Xiao, Wenyan

doi:10.1111/j.1365-313x.2012.05028.x

Cited by 53 publications

(72 citation statements)

References 62 publications

(99 reference statements)

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“…At the phenotypic level, triple knockout/knockdown of the H1 genes leads to developmental abnormalities with a reduction of plant size, delayed flowering, and embryo lethality (Jerzmanowski et al, 2000). Arabidopsis H1s have been found to directly interact with the DNA glycosylase DEMETER, which regulates genomic imprinting by demethylating MEDEA promoter in the endosperm (Rea et al, 2012). Furthermore, loss of H1 alters DNA methylation patterns with different effects on euchromatin and heterochromatin (Wierzbicki and Jerzmanowski, 2005;Zemach et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

The Histone Deacetylase Complex 1 Protein of Arabidopsis Has the Capacity to Interact with Multiple Proteins Including Histone 3-Binding Proteins and Histone 1 Variants

Perrella

Carr²,

Asensi-Fabado³

et al. 2016

Plant Physiol.

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Intrinsically disordered proteins can adopt multiple conformations, thereby enabling interaction with a wide variety of partners. They often serve as hubs in protein interaction networks. We have previously shown that the Histone Deacetylase Complex 1 (HDC1) protein from Arabidopsis (Arabidopsis thaliana) interacts with histone deacetylases and quantitatively determines histone acetylation levels, transcriptional activity, and several phenotypes, including abscisic acid sensitivity during germination, vegetative growth rate, and flowering time. HDC1-type proteins are ubiquitous in plants, but they contain no known structural or functional domains. Here, we explored the protein interaction spectrum of HDC1 using a quantitative bimolecular fluorescence complementation assay in tobacco (Nicotiana benthamiana) epidermal cells. In addition to binding histone deacetylases, HDC1 directly interacted with histone H3-binding proteins and corepressor-associated proteins but not with H3 or the corepressors themselves. Surprisingly, HDC1 also was able to interact with variants of the linker histone H1. Truncation of HDC1 to the ancestral core sequence narrowed the spectrum of interactions and of phenotypic outputs but maintained binding to a H3-binding protein and to H1. Thus, HDC1 provides a potential link between H1 and histone-modifying complexes.Regulation of gene transcription underpins plant development and dynamic responses to the environment. Transcription occurs in the context of chromatin, a highly condensed structure in which the DNA is wrapped around nucleosomes composed of histones H2A/B, H3, and H4 and further stabilized by linker histone H1 (Over and Michaels, 2014;Hergeth and Schneider, 2015). Alteration of chromatin structure plays an important part in transcriptional regulation and is achieved through multiprotein complexes that recognize and instigate biochemical modifications of the DNA and/or the histones (Pfluger and Wagner, 2007;Derkacheva et al., 2013). For example, binding of repressors to so-called corepressors recruits histone deacetylases (HDAs) to the gene region (Song et al., 2005). The HDAs in turn interact with histonebinding proteins (Mehdi et al., 2016). Removal of acetyl groups from Lys residues of the core histones leads to chromatin compaction and inhibition of transcription (Kouzarides, 2007;Roudier et al., 2009). Specific recruitment at both 'ends' of the repressive protein complex generates a double lock between DNA and the nucleosome: the repressors recognize certain DNA motifs in the gene promoters, and the histone-binding proteins recognize ('read') certain histone residues and their modifications (Liu et al., 2010). A minimal HDAC complex therefore needs to combine at least three protein functions: repressor binding, histone binding, and catalytic activity. Biochemical studies in yeast (Saccharomyces cerevisiae) and in animal systems have provided evidence for large multiprotein complexes linking a corepressor and a HDA with several histone-binding proteins and a range of associate...

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Section: Discussionmentioning

confidence: 99%

The Histone Deacetylase Complex 1 Protein of Arabidopsis Has the Capacity to Interact with Multiple Proteins Including Histone 3-Binding Proteins and Histone 1 Variants

Perrella

Carr²,

Asensi-Fabado³

et al. 2016

Plant Physiol.

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“…Mutants h1.1 (SALK_N628430; Rea et al, 2012) and h1.2 (GK-116E080) were obtained from the European Arabidopsis Stock Center. h1.3 in the Ler background was obtained from the Cold Spring Harbor Laboratory collection (GT18298).…”

Section: Plant Materialsmentioning

confidence: 99%

A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis

et al. 2015

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(A.J.).Linker (H1) histones play critical roles in chromatin compaction in higher eukaryotes. They are also the most variable of the histones, with numerous nonallelic variants cooccurring in the same cell. Plants contain a distinct subclass of minor H1 variants that are induced by drought and abscisic acid and have been implicated in mediating adaptive responses to stress. However, how these variants facilitate adaptation remains poorly understood. Here, we show that the single Arabidopsis (Arabidopsis thaliana) stressinducible variant H1.3 occurs in plants in two separate and most likely autonomous pools: a constitutive guard cell-specific pool and a facultative environmentally controlled pool localized in other tissues. Physiological and transcriptomic analyses of h1.3 null mutants demonstrate that H1.3 is required for both proper stomatal functioning under normal growth conditions and adaptive developmental responses to combined light and water deficiency. Using fluorescence recovery after photobleaching analysis, we show that H1.3 has superfast chromatin dynamics, and in contrast to the main Arabidopsis H1 variants H1.1 and H1.2, it has no stable bound fraction. The results of global occupancy studies demonstrate that, while H1.3 has the same overall binding properties as the main H1 variants, including predominant heterochromatin localization, it differs from them in its preferences for chromatin regions with epigenetic signatures of active and repressed transcription. We also show that H1.3 is required for a substantial part of DNA methylation associated with environmental stress, suggesting that the likely mechanism underlying H1.3 function may be the facilitation of chromatin accessibility by direct competition with the main H1 variants.Linker (H1) histones are conserved and ubiquitous structural components of eukaryotic chromatin required for the stabilization of higher order chromatin structure and are generally thought to restrict DNA accessibility. Interestingly, despite their architectural role, H1 histones were shown to be highly mobile and continuously exchanging among chromatin-binding sites (Raghuram et al., 2009). They are also the most variable of the histones, with numerous nonallelic variants coexisting in the same cell. In vertebrates, several evolutionarily conserved subfamilies of H1 can be distinguished (Talbert et al., 2012) and appear to play both redundant and specific roles during development and cellular differentiation (McBryant et al., 2010). There is accumulating evidence that, in animals, regulation of the proportions of H1 variants with different dynamic behavior in chromatin is involved in controlling the accessibility of DNA to trans-acting factors (Jullien et al., 2010;Shahhoseini et al., 2010;Zhang et al., 2012a;Pérez-Montero et al., 2013;Christophorou et al., 2014).Epigenetic mechanisms, including DNA and histone modifications and active nucleosome remodeling, are major players in translating signals about environmental perturbations into adaptive responses at the transc...

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“…Yeast transformants were spotted on synthetic dropout plates without Leu (L) and Trp (W) or without Leu, Trp, and His (H) and with 20 mM 3-aminotriazole (3-AT). The 5-bromo-4-chloro-indolyl-b-Dgalactopyranoside filter-lift assay was as described (Rea et al, 2012). Yeast cultures were serially diluted (103, 1003, and 1,0003).…”

Section: Lno1 Interacts With the Dead-box Helicase/atpase Los4mentioning

confidence: 99%

“…Yeast (Saccharomyces cerevisiae) two-hybrid experiments were performed using the system described previously (Rea et al, 2012). To make Gal4 DNA activation domain (AD) constructs, the full-length LNO1 was PCR amplified with primers LON1-ADF (59-CCCGATATCGATGAGCAGAGTTGAGATTG-AAGAA-39; EcoRV site underlined) and LON1-ADR (59-CCCGTCGACT-CATTTTCTCATCTGTGTGAAGAG-39; SalI site underlined) and inserted into pACT2 vector digested with SmaI and XhoI; the LNO1 N-terminal domain (1-761 amino acids; NTD) coding region was PCR amplified with primers LNO1-NTD-ADF (59-CCCGGATCCGAATGAGCAGAGTTGAGATTGAAG-AA-39; BamHI site underlined) and LNO1-NTD-ADR (59-CCCGTCGACTC-ATATAAACGCGCAAGAATCCTT-39; SalI site underlined) and inserted into pACT2 digested with BamHI and XhoI; the LNO1 DNTD fragment coding region was PCR amplified with primers LNO1-CCC-ADF (59-CCCGATATCGC-TGAAAAGCAATGTTGAAGAACTG-39; EcoRV site underlined) and LON1-ADR and inserted into pACT2 digested with SmaI and XhoI.…”

Section: Yeast Two-hybrid Assaymentioning

confidence: 99%

“…Positive transformants were selected on complete minimal (CM) dropout medium minus Trp and Leu. Positive interactions were selected on CM medium minus Trp, Leu, and His containing 20 mM 3-aminotriazole and were confirmed by filter lift assay (Rea et al, 2012). To further confirm the interactions, a vector-swap experiment was performed.…”

Section: Yeast Two-hybrid Assaymentioning

confidence: 99%

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LONO1Encoding a Nucleoporin Is Required for Embryogenesis and Seed Viability in Arabidopsis

2012

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Early embryogenesis in Arabidopsis (Arabidopsis thaliana) is distinguished by a predictable pattern of cell divisions and is a good system for investigating mechanisms of developmental pattern formation. Here, we identified a gene called LONO1 (LNO1) in Arabidopsis in which mutations can abolish the first asymmetrical cell division of the zygote, alter planes and number of cell divisions in early embryogenesis, and eventually arrest embryo development. LNO1 is highly expressed in anthers of flower buds, stigma papilla of open flowers, and embryo and endosperm during early embryogenesis, which is correlated with its functions in reproductive development. The homozygous lno1-1 seed is not viable. LNO1, a homolog of the nucleoporin NUP214 in human (Homo sapiens) and Nup159 in yeast (Saccharomyces cerevisiae), encodes a nucleoporin protein containing phenylalanineglycine repeats in Arabidopsis. We demonstrate that LNO1 can functionally complement the defect in the yeast temperaturesensitive nucleoporin mutant nup159. We show that LNO1 specifically interacts with the Arabidopsis DEAD-box helicase/ ATPase LOS4 in the yeast two-hybrid assay. Furthermore, mutations in AtGLE1, an Arabidopsis homolog of the yeast Gle1 involved in the same poly(A) mRNA export pathway as Nup159, also result in seed abortion. Our results suggest that LNO1 is a component of the nuclear pore complex required for mature mRNA export from the nucleus to the cytoplasm, which makes LNO1 essential for embryogenesis and seed viability in Arabidopsis.

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Histone H1 affects gene imprinting and DNA methylation in Arabidopsis

Cited by 53 publications

References 62 publications

The Histone Deacetylase Complex 1 Protein of Arabidopsis Has the Capacity to Interact with Multiple Proteins Including Histone 3-Binding Proteins and Histone 1 Variants

The Histone Deacetylase Complex 1 Protein of Arabidopsis Has the Capacity to Interact with Multiple Proteins Including Histone 3-Binding Proteins and Histone 1 Variants

A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNA methylation in Arabidopsis

LONO1Encoding a Nucleoporin Is Required for Embryogenesis and Seed Viability in Arabidopsis

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